Skip to content

Advertisement

  • Research
  • Open Access

Resistance to deltamethrin by domestic and wild Triatoma infestans populations in the municipality of Toro Toro, Potosi, Bolivia

  • 1Email author,
  • 1,
  • 1,
  • 2,
  • 3 and
  • 1
Parasites & Vectors201811:92

https://doi.org/10.1186/s13071-018-2663-5

  • Received: 25 October 2016
  • Accepted: 22 January 2018
  • Published:

Abstract

Background

Chemical control with pyrethroid insecticides has been effective in reducing endemic areas of distribution of Triatoma infestans in the Southern Cone, as well as Bolivia; this had considerably reduced the infestation of households in a large part of the territory. Nowadays, areas such as the Chaco and the Inter-Andean Valleys are regions where the reach of vector control strategies is becoming limited, and infestations of insecticide-treated households are reported more often. The objective of this study was to determine if the persistence of T. infestans stems from changes in the susceptibility of its toxicological profile in four communities in the municipality of Toro Toro, Potosi, Bolivia.

Methods

Susceptibility to deltamethrin of wild and domestic populations of T. infestans was evaluated in two stages (16 populations before and 13 populations after spraying) among DUs (structures in the intra- and peridomicile) and wild ecotopes, in four communities. Serial dilutions of deltamethrin in acetone (0.2 μl) were applied topically on standardized first-stage nymphs. Dose-response results were analyzed with the software PoloPlus and the relationships between lethal doses (LD) and resistance ratios (RR50) were determined.

Results

Different degrees of RR50 were detected among the populations before and after spraying (25.66–54.70 and 21.91–40.67, respectively), as well as in different ecotopes within a DU (DU JC 3, 28.06–36.13, in mixed structures of corrals and chicken coops; and DU JG 3, 46.27–25.70, in kitchen roofs), or in the wild environment of the community JG Sil (29.21–40.67). The mortality of insects undergoing diagnostic dose (DD) was never higher than 34%.

Conclusion

The results obtained in this study showed resistance of T. infestans to deltamethrin in four communities, hence the complexity of this phenomenon is not only limited to the level of communities, but also applies to the microgeographical level, as in different ecotopes present within the DUs. This phenomenon should be considered while planning the activities of control programs.

Keywords

  • Triatoma infestans
  • Bolivia
  • Chagas disease
  • Insecticide resistance
  • Deltamethrin
  • Macro- and microgeography

Background

Chagas disease is an important parasitic infection in Latin America, caused by the parasite Trypanosoma cruzi, mainly transmitted to humans and mammals by blood-sucking triatomine insects [1, 2]. Triatoma infestans Klug (Hemiptera: Reduviidae) is widely distributed in South America [3] and is the main vector species within the endemic area of Bolivia [46]. Insecticides play a central role in controlling major vectors of diseases [7]; control programs in Southern Cone countries focus on the interruption of human T. cruzi transmission by T. infestans, with the application of residual insecticides [8, 9], mainly pyrethroids (particularly deltamethrin) [1012], because of their efficacy, persistence and low environmental impact [1, 13]. But, chemical control was only partially successful in eliminating domestic triatomine infestation.

Resistance to pyrethroids in triatomines has been detected in South America since the 90s [1416]. High levels of resistance to pyrethroids, detected in T. infestans in certain areas of Argentina and Bolivia, were attributed to possible failures of control programs [1721]. In the Chaco region, the success of insecticide control campaigns in rural communities is limited by early reinfestation, apparently originating from residual peridomestic foci [5, 22]. Peridomestic sites are the first to be recolonized, sustain dense populations of T. infestans, and increase the risk of domestic reinfestation in rural northern Argentina [22, 23].

The municipality of Toro Toro (Department of Potosi) is situated in the Bolivia Inter-Andean Valleys. Before the beginning of the Chagas programme in this department, high infestation rates of T. infestans were present. After approximately 15 years of chemical control, the density of T. infestans decreased and achieved a compatible level with the vigilance phase [6]. Nevertheless, T. infestans persists, and it was not known if this was due to operational failures or to susceptible alterations.

Considering previous reports on the different levels of T. infestans resistance in different geographical areas of Bolivia [18, 20, 2427], the objective of this study was to determine if the origin of T. infestans persistence was due to alterations of susceptibility in four communities of the municipality of Toro Toro. Response to insecticide was measured and compared among the different environments (intra, peridomestic and wild environment).

Methods

Study area

The study was carried out in the communities of Taqó Taqó (TQ), Julo Chico (JC), Julo Grande (JG) and Calahuta (CA) of the municipality of Toro Toro (Charcas Province), north of Potosi Department, Bolivia. This area is part of the Bolivian-Tucuman biogeographical province [28, 29]. These communities were historically characterized by high rates of house infestation and high triatomine densities. Since 1995, the infestation has decreased and the area has been under vigilance with irregular control activities using alphacypermethrin. The last insecticide spraying campaign occurred the first quarter of 2013 [30].

In these communities farming is the main form of sustenance, especially guava, lemon and also sweet potato production and animal husbandry (cattle, goats, sheep and poultry). The cultivated areas are restricted and very close to the houses, with a very limited production. Housings are frequently precarious and are built with adobe, stone and the majority of houses have some peridomestic structure to protect the domestic animals (i.e. goat corrals and chicken coops).

A domiciliary unit (DU) was defined as the house (i.e. domestic sites) and structures included within the peridomestic area (e.g. kitchens, corrals, chicken coops); all 95 DU existing were georeferenced and numbered in the four communities TQ (10), JC (25), JG (28) and CA (32). The distances among the communities are between 3–7 km.

The capture of triatomines was carried out in two periods in 2014, January and October (8 months after chemical intervention) by a team composed by two technicians, searching inside houses (intradomicile and peridomestic structures), according to standardized procedures of the Pan American Health Organization [31, 32]. The triatomines were separated in plastic bottles by DUs and ecotopes, and subsequently reared in the laboratory for future analysis.

After the entomological evaluation in the four communities of municipality of Toro Toro, all infested DUs were sprayed with alphacypermethrin at nominal doses of 50 mg a.i./m2, using Hudson X-pertTM manual sprayers, as indicated by the Pan American Health Organization protocol [33].

In parallel to the capture of domestic triatomines, wild populations were collected using traps described by Noireau et al. [34, 35] in ecotopes where the presence of wild triatomines was suspected, in parallel with the capture in the houses. The distance of the sylvatic ecotopes and the nearest houses was between 50–100 m for JC and JG, respectively. The number of traps varied depending on the available sampling area. A total of 30 traps (15 per evaluation) and 100 traps (50 per evaluation) were placed in Julo Chico and Julo Grande, respectively.

All insects collected were identified by using the taxonomic key of Lent & Wygodzinsky [3] and maintained under controlled conditions of temperature and humidity (25 °C ± 1 °C; 60% ± 10% RH).

Chemicals

Deltamethrin technical grade (99.1%), obtained from Bayer CropScience (Brazil), was used for the bioassay, following the routine of “Monitoring Network for Triatominae Insecticide Resistance”, FIOCRUZ [36]. The acetone analytical grade used for dilutions was purchased from Merck, Germany. To test the susceptibility to insecticide, the triatomine colonies were founded after each phase of the work from a minimum of five insects [37] captured in the two phases of the work described in Table 1.
Table 1

Number of T. infestans captured in the domestic and sylvatic ecotopes, in four communities of Toro Toro, Potosi, Bolivia, before and after spraying (January and October 2014)

Community

Houses

Before spraying

After spraying

 

No. visited

No. positive

Intra (n)

Peri (n)

Wild (n)

Intra (n)

Peri (n)

Wild (n)

Taqó Taqó

10

1

0

48

0

0

3

0

Julo Chico

25

7

24

46

12

0

106

0

Julo Grande

28

6

31

10

11

57

27

5

Calahuta

32

5

3

123

0

0

26

0

Abbreviations: Intra intradomestic, Peri peridomestic, n number of individuals

Bioassays

Although the chemical control in the municipality of Toro Toro is performed with alphacypermethrin, in the present work bioassays were realized using deltamethrin as reference insecticide, following the routine of the Laboratory of Reference in Triatomines and Epidemiology of Chagas Disease, FIOCRUZ, Belo Horizonte. Reference Center in Triatomine Resistance Studies for the Brazilian Ministry of Health and is recognized as a Collaborator Center for WHOPES.

The susceptible reference lineage (SRL) CIPEIN came from Centro de Investigaciones de Plagas e Insecticidas (CIPEIN) [38]. The baseline of susceptibility to deltamethrin of this lineage was determined by Gomez et al. [25] in Laboratory of Reference in Triatomines and Epidemiology of Chagas Disease, FIOCRUZ, Belo Horizonte.

Tests to determine insecticide susceptibility were conducted for each population; where a minimum of eight and a maximum thirteen doses by populations of active ingredient (a.i.), were applied ranging from 0.42 to 55 ng. For each insecticide dose, three replicates were performed with 10 instar F1 generation nymphs (five days, fasting, weight of 1.2 ± 0.2 mg). The topical application was through 0.2 μl of insecticide dilution in the dorsal abdomen, according to the procedures of the World Health Organization [39] and Pessoa et al. [40]. After treatment, mortality was assessed 72 h post-application and determined by the inability or lack of coordination of the nymphs to move from center to the edge of the filter paper (7 cm diameter). Signs of paralysis and lack of response to external stimuli were also considered. During and after the experiment, insects were kept under controlled conditions of temperature and relative humidity (25 °C ± 1 °C; 60% ± 10% RH).

Diagnostic dose

The diagnostic doses (DD) applied was twice the minimum of the insecticide that causes 99% of mortality in the susceptible laboratory strain [20, 25, 41]. According to Gomez et al. [25] the LD99 to deltamethrin of the SRL was determined (5.50 ng a.i per insect) and the DD was estimated. According to Brown & Pal [42], mortality > 80% (DD) detects the presence of resistant individuals in a population. Values of RR50 > 5, according to the criteria established by PAHO [43], were considered as resistant to deltamethrin.

Data analysis

The dose data/mortality was analyzed using the program PoloPlus version 2.0 [44]. The lethal doses required to kill 50% of treated individuals (LD50) was estimated and the resistance ratio (RR50), with their respective confidence intervals (95% CI).

Results

In the four communities, 305 and 221 triatomines were captured before and after spraying, respectively. All captured triatomines were identified as T. infestans. Nineteen DUs were infested in the first phase and 11 in the second phase of the study (7 DUs were recurrent of the first phase). Two sylvatic foci were found, one in the communities of JC and another in JG; after eight months, only JG was positive in the second phase (Table 1).

Sixteen samples were obtained in the first capture, defined by the different domestic structures in the intra and peridomestic environments, and two in the sylvatic environments. All populations were resistant to deltamethrin (Table 2). The values of RR50 were 28.90 in the intradomicile to 54.7 for the peridomicile, and the wild population showed RR50 of 29.21–38.21. In the second capture of 13 populations of T. infestans from domestic and wild environments, all were resistant to deltamethrin (Table 3), with values RR50 of 21.91–40.67.
Table 2

Toxicological profile of T. infestans populations of domestic and sylvatic ecotopes, evaluated in the communities of Taqó Taqó, Julo Chico, Julo Grande and Calahuta, Potosi, Bolivia, before spraying with alphacypermethrin 50 mg a.i./m2 (January 2014)

CD

Ecotope (I, P, S)

Before spraying

  

LD50 (95% CI) (n)

Slope ± SE

RR50 (95% CI)

(n) DD%

CIPEIN (SRL)

 

0.47 (0.32–0.51) (210)

3.03 ± 0.37

  

TQ 1

Goat corral (P)

12.78 (10.88–14.59) (216)

3.80 ± 0.44

31.37 (25.08–39.25)

(30)14.8

JC 2

Kitchen wall (P)

12.33 (9.9–14.6) (270)

2.57 ± 0.32

30.26 (23.46–39.03)

(30) 23.3

JC 3(a)

Deposit (P)

11.43 (10.01–12.81) (270)

3.57 ± 0.39

28.06 (22.75–34.61)

(30) 13.3

JC 3(b)

Goat corral and chicken coop (P)a

22.29 (20.04–24.59) (300)

4.06 ± 0.40

54.70 (44.83–66.73)

(30) 0

JC 4

Goat corral (P)

12.41 (8.37–16.98) (240)

2.73 ± 0.32

30.47 (24.06–38.60)

(30) 23.3

JC 7

Chicken coop (P)

13.06 (10.734–15.26) (240)

2.74 ± 0.35

32.06 (25.15–40.87)

(30) 23.3

JC Sil

Rocky outcrop (S)

15.57 (14.09–17.07) (300)

4.54 ± 0.43

38.21 (31.42–46.47)

(30) 3.3

JG 1

Goat corral (P)

10.45 (9.11–11.84) (300)

3.09 ± 0.31

25.66 (20.69–31.81)

(30) 16.7

JG 3

Kitchen roof (P)

18.85 (16.79–20.84) (240)

4.02 ± 0.53

46.27 (37.85–56.57)

(30) 0

JG 4(a)

Bedroom (I)

14.72 (13.28–16.24) (300)

3.98 ± 0.38

36.12 (29.63–44.04)

(30) 0

JG 6

Bedroom (I)

11.77 (10.55–12.99) (240)

4.76 ± 0.49

28.90 (23.67–35.28)

(30) 6.6

JG Sil

Rock cliff (S)

11.90 (10.55–13.25) (270)

4.14 ±0.41

29.21 (23.80–35.86)

(30) 6.6

CA 1

Living room wall (P)

13.27 (11.64–14.90) (390)

3.00 ± 0.27

32.57 (26.38–40.22)

(30) 6.6

CA 2

Living room wall (P)

22.28 (17.97–27.34) (270)

3.36 ± 0.38-

54.67 (44.42–67.29)

(30) 0

CA 5(a)

Goat corral (P)

15.63 (13.99–17.23) (300)

4.36 ± 0.43

38.35 (31.41–46.82)

(30) 3.3

CA 5(b)

Dog house (P)

15.99 (14.64–17.39) (240)

5.53 ±0.57

39.25 (32.43–47.50)

(30) 0

Abbreviations: CD code triatomine population, SRL susceptible reference lineage, I intradomestic, P peridomestic, S sylvatic, n number of individuals used, LD 50 lethal dose that killed 50% of the population (ng.a.i./insect), CI confidence interval, RR 50 resistance ratio, DD % mortality at the diagnostic dose

aMixed structure of goat corral and chicken coop

Table 3

Toxicological profile of T. infestans populations of domestic and sylvatic ecotopes, evaluated in the communities of Julo Chico, Julo Grande and Calahuta, Potosi, Bolivia, after spraying with alphacypermethrin 50 mg a.i./m2 (October 2014)

CD

Ecotope (I, P, S)

After spraying

  

LD50 (95% CI) (n)

Slope ± SE

RR50 (95% CI)

(n) DD%

CIPEIN (SRL)

 

0.47 (0.32–0.51) (210)

3.03 ± 0.37

  

JC 2

Kitchen wall (P)

12.11 (10.40–13.81) (270)

3.17 ± 0.34

29.72 (23.81–37.08)

(30) 6.7

JC 3(b)

Goat corral and chicken coop (P)a

14.72 (11.95–17.37) (240)

3.55 ± 0.42

36.13 (29.07–44.90)

(30) 13.3

JC 8

Goat corral (P)

11.10 (9.38–12.68) (270)

3.40 ± 0.39

27.26 (21.74–34.18)

(30) 10

JG 3

Kitchen roof (P)

10.47 (6.66–13.75) (180)

2.89 ± 0.44

25.70 (19.93–33.15)

(30) 30

JG 4(a)

Bedroom (I)

14.44 (10.72–17.94) (270)

2.51 ± 0.30

35.45 (27.66–45.43)

(30) 13.3

JG 4(b)

Tree with chickens (P)

12.71 (10.32–14.90) (270)

2.72 ± 0.33

31.19 (24.34–39.96)

(30) 13.3

JG 4(c)

Chicken coop (P)

10.22 (8.47–11.84) (180)

3.59 ± 0.48

25.10 (19.82–31.78)

(30) 16.7

JG 5

Bedroom wall (P)

11.03 (7.80–13.93) (210)

3.49 ± 0.43

27.08 (21.49–34.12)

(30) 23.3

JG 6

Bedroom (I)

11.34 (9.19–13.32) (210)

2.92 ± 0.40

27.84 (21.72–35.68)

(30) 13.3

JG Sil

Rock cliff (S)

16.57 (10.86–22.19) (270)

2.45 ± 0.32

40.67 (32.04–51.64)

(30) 20.0

CA 2

Living room wall (P)

11.34 (9.12–13.37) (210)

3.80 ± 0.39

27.83 (21.63–35.80)

(30) 23.3

CA 3

Goat corral (P)

8.92 (5.09–11.67) (180)

3.41 ± 0.54

21.91 (17.23–27.85)

(30) 33.3

CA 5(a)

Goat corral (P)

16.51 (12.55–19.97) (210)

5.88 ± 0.72

40.52 (33.41–49.15)

(30) 3.3

Abbreviations: CD code triatomine population, SRL susceptible reference lineage, I intradomestic, P peridomestic, S sylvatic, n number of individuals used, LD 50 lethal dose that killed 50% of the population (ng.a.i./insect), CI confidence interval, RR 50 resistance ratio, DD % mortality of the diagnostic dose

aMixed structure of goat corral and chicken coop

All populations evaluated before and after spraying showed mortality lower than 33% for the diagnostic dose (DD). Comparing before and after spraying at the microgeographical level, the toxic response was different for triatomines within the same DU in the different communities. Of the seven DU positives (before and after fumigation), four had similar values of (JC2, JG4a, JG6, CA5a) and in three DUs, lower resistance after spraying (JC3b, JG3, CA2) was observed (Tables 2 and 3).

Discussion

This study shows the high resistance to deltamethrin by domestic and wild T. infestans populations in four communities of the municipality of Toro Toro, Bolivia, before and eight months after spraying. Of particular importance are the results at the microgeographical level, demonstrating different resistance values in structures of the same DU. The calculation of RR50 is an important and frequent indicator of triatomine resistance to insecticides besides the diagnostic dose DD [17, 20, 25, 45], as it provides information about the mortality of a population in contact with different doses of insecticide, and can be employed to detect the presence of resistant individuals in a population [42]. How these indicators vary was evidenced in our measurements in an artificial environment (a mixed structure used as goat corral and chicken coop) before and after spraying: housing 3(b) of Julo Chico had a RR50 of 54.7 and RR50 of 36.13, contrary to what was observed in environments intradomicile of the house 4(a) of Julo Grande (RR50 of 36.12 to RR50 of 35.45). The variation in the wild environment of Julo Chico (RR50 of 38.21) and Julo Grande (RR50 of 29.21 to RR50 of 40.67) was also variable.

There was also variation in the values observed inside the same house (house 3 of Julo Chico), among the insects captured in different ecotypes and in the same period: deposit with RR50 of 28.6 and goat corral and chicken coop with RR50 of 54.7.

These different resistance profiles in different DUs from the same communities show the different geographical structuring of the resistance phenotype among the communities and ecotypes within sites at the microgeographical level. Already among the wild populations these showed profiles of high insecticide resistance. Thus, the persistence of these residual foci is probably related to the low efficiency of the insecticide applied in these communities. According to what was observed in areas of the Gran Chaco, both environmental factors [22, 46, 47] and existing surface characteristics would have different effects on the applied insecticide, conditioning or limiting its insecticidal action. In this situation, the insects would be exposed to sublethal doses, selecting resistant insects [13, 48, 49].

On the other hand, studies of T. infestans wild populations indicate that diverse regions of Bolivia [25, 26, 49] present different resistance profiles to insecticides. Wild populations from the Inter-Andean Valleys (Andean region) and the Gran Chaco (non-Andean region) resulted in resistance to deltamethrin with values ranging between 6.8 and 11.9 [26, 48]. Fipronil resistance varies between 5.5–45.6 [26], although this insecticide has never been used to triatomine control. In parallel, in these regions other wild T. infestans populations were reported susceptible [25].

Our results of wild T. infestans population showed high rates of resistance, ranging between 29.21–40.67. According to our observations and information from local authorities, the sylvatic area studied has never presented anthropogenic changes (such as agriculture or pasture), due its topography with predominance of rocky hills. As described in other regions, it seems that this deltamethrin resistance could be autochthonous, and the origin of the resistant domiciliary insects. The other way, from the houses to the sylvatic environment, had never been described for T. infestans. Nonetheless, it must be investigated using molecular markers.

Conversely, the presence of different profiles of residual foci of T. infestans in Bolivia indicates the occurrence of independent evolutionary processes of resistance to insecticides in the different regions. The high genetic variability described for T. infestans by Torres-Perez et al. [50] and Panzera et al. [51] justifies Bolivia as the center of origin and dispersion of the species, which could explain the reason why natural insecticides resistance have risen in this country [52].

Conclusions

The results of the present study demonstrated high resistance to deltamethrin of domestic and sylvatic T. infestans of Toro Toro, Potosi, Bolivia, varying at the macro- and microgeographical levels; this is more complex when considering the importance of many factors that act over the biological performance of a population, e. g. reproductive capacity, viable offspring, obtaining blood capacity, dispersion capacity, and others, that should be investigated.

Abbreviations

a.i.: 

active ingredient

RH: 

relative humidity

Declarations

Acknowledgments

This study was supported by PEC-PG Capes/Brazil through granting of a doctoral scholarship (15254-12-7) to JEE. We thank to the National Chagas Disease to Bolivia, Lic. Omar Tenorio Vasquez for assistance in the collection of Triatominae on the field and Dr Luis Eduardo Martínez Villegas for the correction of English; to Bayer S.A. Brazil for providing the insecticide (deltamethrin technical grade 99.1%); to the CIPEIN, for the susceptible reference lineage (SRL).

Funding

Not applicable.

Availability of data and materials

All data generated or analysed during this study are included in this published article.

Authors’ contributions

All the authors have contributed substantially to this study. JEE, LGD, MBG and MRC conceived the study. JEE, MBG and ANR compiled the data. JEE and MBG analyzed the data. JEE, LGD, GCDP and MBG wrote the paper. All authors read and approved the final manuscript.

Ethics approval and consent to participate

This study was carried out in strict accordance with the recommendations in the Guide of the Ethics Committee of Fundação Oswaldo Cruz. The protocol was approved by the Comissão de Ética no Uso de Animais (CEUA-Fiocruz, Permit Number: 41/14-2). The weekly feeding on chicken (Gallus gallus) was performed using detomidine + ketamine anesthesia (intramuscular injection).

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Laboratório de Referência Triatomíneos e Epidemiologia da Doença de Chagas, Centro de Pesquisas René Rachou, FIOCRUZ-M G, Belo Horizonte, Brasil
(2)
CEADES Salud y Medio Ambiente/Plataforma Chagas, Cochabamba, Bolivia
(3)
Servicio Departamental de Salud - Potosi, Programa Nacional de Chagas, Potosi, Bolivia

References

  1. Dias J, Schofield CJ. The evolution of Chagas disease (American trypanosomiasis) control after 90 years since Carlos Chagas discovery. Mem Inst Oswaldo Cruz. 1999;94:103–21.View ArticlePubMedGoogle Scholar
  2. Waleckx E, Suarez J, Richards B, Dorn PL. Triatoma sanguisuga blood meals and potential for Chagas disease, Louisiana, USA. Emerg Infect Dis. 2014;20:2141–3.View ArticlePubMedPubMed CentralGoogle Scholar
  3. Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera, Reduviidae), and their significance as vectors of Chagas’ disease. Bull Am Mus Nat Hist. 1979;163:125–520.Google Scholar
  4. Romaña C. Enfermedad de Chagas. Buenos Aires: López Libreros; 1963.Google Scholar
  5. Guillén G, Diaz R, Jemio A, Cassab JA, Pinto CT, Schofield CJ. Chagas disease vector control in Tupiza, southern Bolivia. Mem Inst Oswaldo Cruz. 1997;92:1–8.Google Scholar
  6. Programa Nacional de Control de Chagas (PNCCH). Anuario Programa Nacional de Chagas Bolivia. In: La Paz: Estado Plurinacional de Bolivia Ministerio de Salud y Deportes Dirección General de Servicios de Salud Unidad de Epidemiologia Programa Nacional de Chagas; 2008.Google Scholar
  7. Hemingway J, Ranson H. Insecticide resistance in insect vectors of human disease. Annu Rev Entomol. 2000;45:371–91.View ArticlePubMedGoogle Scholar
  8. Schofield C. Field testing and evaluation of insecticides for indoor residual spraying against domestic vectors of Chagas disease: World Health Organization, Communicable Disease Control, Prevention and Eradication, WHO Pesticide Evaluation Scheme. 2001. http://apps.who.int/iris/bitstream/10665/66782/1/WHO_CDS_WHOPES_GCDPP_2001.1.pdf. Accessed 20 Sept 2016.Google Scholar
  9. Dias JCP, Silveira AC, Schofield CJ. The impact of Chagas disease control in Latin America: a review. Mem Inst Oswaldo Cruz. 2002;97:603–12.View ArticlePubMedGoogle Scholar
  10. Zerba E. Susceptibility and resistance to insecticides of Chagas disease vectors. Medicina. 1999;59:41–6.PubMedGoogle Scholar
  11. Schofield CJ, Jannin J, Salvatella R. The future of Chagas disease control. Trends Parasitol. 2006;22:583–8.View ArticlePubMedGoogle Scholar
  12. Dias JCP. Southern Cone Initiative for the elimination of domestic populations of Triatoma infestans and the interruption of transfusion Chagas disease: historical aspects, present situation, and perspectives. Mem Inst Oswaldo Cruz. 2007;102:11–8.View ArticlePubMedGoogle Scholar
  13. Gürtler RE. Research Directly Linked With Current Vector Control Strategy. Working paper for the Scientific Working Group on Chagas Disease Research, convened by the Special Programme for Research and Training in Tropical Diseases (TDR) and the Pan American Health Organization (PAHO). 2007. http://citeseerx.ist.psu.edu/viewdoc/download?doi=10.1.1.596.3086&rep=rep1&type=pdf. Accessed 28 Sept 2016.
  14. Vassena C, Picollo M, Zerba E. Insecticide resistance in Brazilian Triatoma infestans and Venezuelan Rhodnius prolixus. Med Vet Entomol. 2000;14:51–5.View ArticlePubMedGoogle Scholar
  15. Santo Orihuela PL, Vassena CV, Zerba EN, Picollo MI. Relative contribution of monooxygenase and esterase to pyrethroid resistance in Triatoma infestans (Hemiptera: Reduviidae) from Argentina and Bolivia. J Med Entomol. 2008;45:298–306.View ArticleGoogle Scholar
  16. Pessoa GCD, Vinãs PA, Rosa ACL, Diotaiuti L. History of insecticide resistance of Triatominae vectors. Rev Soc Bras Med Trop. 2015;48:380–9.View ArticlePubMedGoogle Scholar
  17. Picollo MI, Vassena C, Santo Orihuela P, Barrios S, Zaidemberg M, Zerba E. High resistance to pyrethroid insecticides associated with ineffective field treatments in Triatoma infestans (Hemiptera: Reduviidae) from northern Argentina. J Med Entomol. 2005;42:637–42.View ArticlePubMedGoogle Scholar
  18. Toloza AC, Germano M, Cueto GM, Vassena C, Zerba E, Picollo MI. Differential patterns of insecticide resistance in eggs and first instars of Triatoma infestans (Hemiptera: Reduviidae) from Argentina and Bolivia. J Med Entomol. 2008;45:421–6.View ArticlePubMedGoogle Scholar
  19. Germano M, Acevedo GR, Cueto GM, Toloza A, Vassena C, Picollo M. New findings of insecticide resistance in Triatoma infestans (Heteroptera: Reduviidae) from the Gran Chaco. J Med Entomol. 2010;47:1077–81.View ArticlePubMedGoogle Scholar
  20. Lardeux F, Depickère S, Duchon S, Chavez T. Insecticide resistance of Triatoma infestans (Hemiptera, Reduviidae) vector of Chagas disease in Bolivia. Trop Med Int Health. 2010;15:1037–48.PubMedGoogle Scholar
  21. Gurevitz JM, Gaspe MS, Enriquez GF, Provecho YM, Kitron U, Gürtler RE. Intensified surveillance and insecticide-based control of the Chagas disease vector Triatoma infestans in the Argentinean Chaco. PLoS Negl Trop Dis. 2013;7:e2158.View ArticlePubMedPubMed CentralGoogle Scholar
  22. Cécere MC, Gürtler RE, Canale D, Chuit R, Cohen JE. The role of the peridomiciliary area in the elimination of Triatoma infestans from rural Argentine communities. Rev Panam Salud Públ. 1997;1:273–9.View ArticleGoogle Scholar
  23. Cécere M, Gürtler R, Canale D, Chuit R, Cohen J. Effects of partial housing improvement and insecticide spraying on the reinfestation dynamics of Triatoma infestans in rural northwestern Argentina. Acta Trop. 2002;84:101–16.View ArticlePubMedGoogle Scholar
  24. Quisberth S, Waleckx E, Monje M, Chang B, Noireau F, Brenière SF. “Andean” and “non-Andean” ITS-2 and mtCytB haplotypes of Triatoma infestans are observed in the Gran Chaco (Bolivia): population genetics and the origin of reinfestation. Infect Genet Evol. 2011;11:1006–14.View ArticlePubMedGoogle Scholar
  25. Gomez MB, Pessoa G, Orellana ALG, Cortez MR, Rosa ACL, Noireau F. Susceptibility to deltamethrin of wild and domestic populations of Triatoma infestans of the Gran Chaco and the Inter-Andean valleys of Bolivia. Parasit Vectors. 2014;7:497.Google Scholar
  26. Acevedo GR, Cueto GM, Germano M, Orihuela PS, Cortez MR, Noireau F, et al. Susceptibility of sylvatic Triatoma infestans from Andeans valleys of Bolivia to deltamethrin and fipronil. J Med Entomol. 2011;48:828–35.View ArticleGoogle Scholar
  27. Germano MD. Herencia y efectos demográficos de la resistencia a deltametrina en Triatoma infestans. 2012. http://digital.bl.fcen.uba.ar/gsdl-282/cgi-bin/library.cgi?a=d&c=tesis&d=Tesis_5316_Germano. Accessed 28 Sept 2013.Google Scholar
  28. Antezana C, Navarro G. Contribución al análisis biogeográfico y catálogo preliminar de la flora de los valles secos interandinos del centro de Bolivia. Rev Bol de Ecol Bolivia. 2002;12:3–38.Google Scholar
  29. Navarro G. Provincia Biogeografía de la Puna Peruana. In: Navarro G, Maldonado M, editors. Geografía ecológica de Bolivia: Vegetación y ambientes acuáticos. Centro de Ecología Simón I. Patiño. Cochabamba: Departamento de Difusión; 2002. p. 243–451.Google Scholar
  30. Programa Nacional de Control de Chagas (PNCCH). Relatorio técnico. In: Programa Nacional de Chagas, Departamento de Potosi, Bolivia; 2013.Google Scholar
  31. Silveira AC, Sanches O. Guía para muestreo en actividades de vigilancia y control vectorial de la enfermedad de Chagas. 2003. http://www.paho.org/uru/index.php?gid=57&option=com_docman&task=doc_view. Accessed 15 Feb 2011.Google Scholar
  32. Programa Nacional de Control de Chagas-Escudo Epidemiológico, Ministerio de Salud y Deporte. Manual de Operaciones de Campo. In: Programa Nacional de Control de Chagas Ministerio de Salud y Deporte, La Paz-Bolivia; 2000. p. 53.Google Scholar
  33. World Health Organization. Pesticides and their application: for the control of vectors and pests of public health importance. 6th ed; 2006. http://whqlibdoc.who.int/hq/2006/WHO_CDS_NTD_WHOPES_GCDPP_2006.1_eng.pdf. Accessed 25 June 2015Google Scholar
  34. Noireau F. La enfermedad de Chagas y sus particularidades epidemiológicas en Bolivia. Chagas, la enfermedad en Bolivia: conocimientos científicos al inicio del programa de control (1998–2002), La Paz; 1999. p. 17–47.Google Scholar
  35. Noireau F, Abad-Franch F, Valente SA, Dias-Lima A, Lopes CM, Cunha V, et al. Trapping Triatominae in silvatic habitats. Mem Inst Oswaldo Cruz. 2002;97:61–3.View ArticlePubMedGoogle Scholar
  36. Pessoa GC, Alburquerque R, Alves RV, da Costa VM, Cavalcante KR, Diotaiuti L. Fortalecimento da vigilância em saúde no Brasil: Rede de Monitoramento da Resistência dos triatomíneos aos inseticidas. Rev Patoa Trop. 2016;45:417–24.View ArticleGoogle Scholar
  37. Amelotti I, Romero N, Catalá SS, Gorla DE. Variability of the susceptibility to deltamethrin in Triatoma infestans: the female factor. J Med Entomol. 2011;48:1167–73.View ArticlePubMedGoogle Scholar
  38. Picollo M, Wood E, Zerba E, Licastro S, Ruveda M. Métodos de laboratorio para medir la actividad de insecticidas en Triatoma infestans. Acta Bioquim Clin Latinoam. 1976;10:67–71.Google Scholar
  39. World Health Organization. Protocolo de evaluación de efecto insecticida sobre triatominos. Acta Toxicol Arg. 1994;2:29–32.Google Scholar
  40. Pessoa GCD, Santos TRM, Salazar GC, Dias LS, Mello BV, Ferraz ML, Diotaiuti L. Variability of susceptibility to deltamethrin in peridomestic Triatoma sordida from Triângulo Mineiro, State of Minas Gerais, Brazil. Rev Soc Bras Med Trop. 2015;48:417–21.View ArticlePubMedGoogle Scholar
  41. World Health Organization. Guidelines for testing mosquito adulticides for indoor residual spraying and treatment of mosquito nets, vol. 60; 2006. http://apps.who.int/iris/bitstream/10665/69296/1/WHO_CDS_NTD_WHOPES_GCDPP_2006.3_eng.pdf. Accessed 2 June 2016Google Scholar
  42. Brown AWA, Pal R. Résistance des arthropodes aux insecticides, 2nd ed., Série de Monographies 38. Geneve: Organisation Mondiale de la Santé; 1973. p. 541.Google Scholar
  43. Organización Panamericana de la Salud. II Reunion técnica latinoamericana de monitoreo de resistência a insecticidas em triatominos vectores de Chagas, OPS. Panamá: PAHO; 2005.Google Scholar
  44. Software. L. PoloPlus: probit and logit analysis. In: LeOra Software: Berkeley, CA; 2002.Google Scholar
  45. Depickère S, Buitrago R, Siñani E, Baune M, Monje M, Lopez R, Waleckx E, et al. Susceptibility and resistance to deltamethrin of wild and domestic populations of Triatoma infestans (Reduviidae: Triatominae) in Bolivia: new discoveries. Mem Inst Oswaldo Cruz. 2012;107:1042–7.View ArticlePubMedGoogle Scholar
  46. Rojas de Arias A, Lehane M, Schofield C, Maldonado M. Pyrethroid insecticide evaluation on different house structures in a Chagas disease endemic area of the Paraguayan Chaco. Mem Inst Oswaldo Cruz. 2004;99:657–62.View ArticlePubMedGoogle Scholar
  47. Germano MD, Picollo MI, Mougabure-Cueto GA. Microgeographical study of insecticide resistance in Triatoma infestans from Argentina. Acta Trop. 2013;128:561–565.Google Scholar
  48. Gürtler RE. Sustainability of vector control strategies in the Gran Chaco Region: current challenges and possible approaches. Mem Inst Oswaldo Cruz. 2009;104:52–9.View ArticlePubMedPubMed CentralGoogle Scholar
  49. Cécere MC, Vazquez-Prokopec GM, Gürtler RE, Kitron U. Spatio-temporal analysis of reinfestation by Triatoma infestans (Hemiptera: Reduviidae) following insecticide spraying in a rural community in northwestern Argentina. Am J Trop Med Hyg. 2004;71:803–10.PubMedPubMed CentralGoogle Scholar
  50. Torres-Perez F, Acuna-Retamar M, Cook JA, Bacigalupo A, García A, Cattan PE. Statistical phylogeography of Chagas disease vector Triatoma infestans: testing biogeographic hypotheses of dispersal. Infect Genet Evol. 2011;11:167–74.View ArticlePubMedGoogle Scholar
  51. Panzera F, Ferreiro MJ, Pita S, Calleros L, Pérez R, Basmadjián Y, et al. Evolutionary and dispersal history of Triatoma infestans, main vector of Chagas disease, by chromosomal markers. Infect Genet Evol. 2014;27:105–13.View ArticlePubMedGoogle Scholar
  52. Dias JP, Schofield CJ. Introducción. Triatominos de Bolivia y la enfermedad de Chagas. In: Cortez MR, editor. Triatominos de Bolivia y la enfermedad de Chagas “Triatoma infestans, principal vector de la enfermedad de Chagas en Bolívia. Ministerio de Salud y Deportes de Bolivia-Programa Nacional de Chagas; 2007. p. 15–7.Google Scholar

Copyright

© The Author(s). 2018

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate. Please note that comments may be removed without notice if they are flagged by another user or do not comply with our community guidelines.

Advertisement